Chemosensory cues to conspecific emotional stress activate amygdala in humans

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Mujica Parodi, Lilianne R ^a   Strey, Helmut H ^a   Frederick, Blaise ^b   Savoy, Robert ^b   Cox, David ^c   Botanov, Yevgeny ^a   Tolkunov, Denis ^a   Rubin, Denis ^a   Weber, Jochen ^d  

^a STONY BROOK UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; ASSOCIATION; BEHAVIOR CHANGE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; EMOTIONAL STRESS; EXERCISE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; NEUROIMAGING; OLFACTORY DISCRIMINATION; PSYCHOMETRY; SIGNAL DETECTION; SWEATING; EMOTION; MENTAL STRESS; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY;

MAMMALIA;

AMYGDALA; EMOTIONS; HUMANS; MAGNETIC RESONANCE IMAGING; STRESS, PSYCHOLOGICAL;

EID: 68149141708     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006415     Document Type: Article

References (73)

1. Pfeiffer W (1963) Alarm substances. Experientia 19: 113-123.
2. Kiyokawa Y, Shimozuru M, Kikusui T, Takeuchi Y, Mori Y (2006) Alarm pheromone increases defensive and risk assessment behaviors in male rats. Physiol Behav 87: 383-387.
3. Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2005) Mapping the neural circuit activated by alarm pheromone perception by c-Fos immunohistochemistry. Brain Res 1043: 145-154.
4. Inagaki H, Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2008) Enhancement of the acoustic startle reflex by an alarm pheromone in male rats. Physiol Behav 93: 606-611.
5. Wysocki CJ, Preti G (2004) Facts, fallacies, fears, and frustrations with human pheromones. Anat Rec A Discov Mol Cell Evol Biol 281: 1201-1211.
6. McClintock MK (1971) Menstrual synchorony and suppression. Nature 229: 244-245.
7. Stern K, McClintock MK (1998) Regulation of ovulation by human pheromones. Nature 392: 177-179.
8. Wyart C, Webster WW, Chen JH, Wilson SR, McClary A, et al. (2007) Smelling a single component of male sweat alters levels of cortisol in women. J Neurosci 27: 1261-1265.
9. Grosser BI, Monti-Bloch L, Jennings-White C, Berliner DL (2000) Behavioral and electrophysiological effects of androstadienone, a human pheromone. Psychoneuroendocrinology 25: 289-299.
10. Jacob S, Hayreh DJ, McClintock MK (2001) Context-dependent effects of steroid chemosignals on human physiology and mood. Physiol Behav 74: 15-27.
11. Jacob S, Kinnunen LH, Metz J, Cooper M, McClintock MK (2001) Sustained human chemosignal unconsciously alters brain function. Neuroreport 12: 2391-2394.
12. Jacob S, Garcia S, Hayreh D, McClintock MK (2002) Psychological effects of musky compounds: comparison of androstadienone with androstenol and muscone. Horm Behav 42: 274-283.
13. Savic I, Berglund H, Gulyas B, Roland P (2001) Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 31: 661-668.
14. Lundstrom JN, Goncalves M, Esteves F, Olsson MJ (2003) Psychological effects of subthreshold exposure to the putative human pheromone 4,16-androstadien-3-one. Horm Behav 44: 395-401.
15. Lundstrom JN, Olsson MJ, Schaal B, Hummel T (2006) A putative social chemosignal elicits faster cortical responses than perceptually similar odorants. Neuroimage 30: 1340-1346.
16. Bensafi M, Tsutsui T, Khan R, Levenson RW, Sobel N (2004) Sniffing a human sex-steroid derived compound affects mood and autonomic arousal in a dose-dependent manner. Psychoneuroendocrinology 29: 1290-1299.
17. Lundstrom JN, Olsson MJ (2005) Subthreshold amounts of social odorant affect mood, but not behavior, in heterosexual women when tested by a male, but not a female, experimenter. Biol Psychol 70: 197-204.
18. Villemure C, Bushnell MC (2007) The effects of the steroid androstadienone and pleasant odorants on the mood and pain perception of men and women. Eur J Pain 11: 181-191.
19. Chen D, Haviland-Jones J (2000) Human olfactory communication of emotion. Perceptual & Motor Skills 91: 771-781.
20. Ackerl K, Atzmueller M, Grammer K (2002) The scent of fear. Neuroendocrinology Letters 23: 79-84.
21. Chen D, Katdare A, Lucas N (2006) Chemosignals of fear enhance cognitive performance in humans. Chem Senses 31: 415-423.
22. Zhou W, Chen D (2009) Fear-related chemosignals modulate recognition of fear in ambiguous facial expressions. Psychol Sci 20: 177-183.
23. Pause BM, Ohrt A, Prehn A, Ferstl R (2004) Positive emotional priming of facial affect perception in females is diminished by chemosensory anxiety signals. Chem Senses 29: 797-805.
24. Prehn A, Ohrt A, Sojka B, Ferstl R, Pause BM (2006) Chemosensory anxiety signals augment the startle reflex in humans. Neurosci Lett 394: 127-130.
25. LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23: 727-738.
26. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48: 175-187.
27. Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16: 331-348.
28. Zald DH, Pardo JV (2000) Functional neuroimaging of the olfactory system in humans. Int J Psychophysiol 36: 165-181.
29. Kevetter GA, Winans SS (1981) Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the "vomeronasal amygdala". J Comp Neurol 197: 81-98.
30. Yokosuka M, Matsuoka M, Ohtani-Kaneko R, Iigo M, Hara M, et al. (1999) Female-soiled bedding induced fos immunoreactivity in the ventral part of the premammillary nucleus (PMv) of the male mouse. Physiol Behav 68: 257-261.
31. Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, et al. (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6: 196-202.
32. Winston JS, Gottfried JA, Kilner JM, Dolan RJ (2005) Integrated neural representations of odor intensity and affective valence in human amygdala. J Neurosci 25: 8903-8907.
33. Klein SA (2001) Measuring, estimating, and understanding the psychometric function: a commentary. Percept Psychophys 63: 1421-1455.
34. Adolphs R (2004) Emotional vision. Nat Neurosci 7: 1167-1168.
35. Amaral DG (2002) The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety. Biol Psychiatry 51: 11-17.
36. Buchel C, Dolan RJ, Armony JL, Friston KJ (1999) Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. J Neurosci 19: 10869-10876.
37. Buchel C, Morris J, Dolan RJ, Friston KJ (1998) Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20: 947-957.
38. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA (1998) Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20: 937-945.
39. Phelps EA, O'Connor KJ, Gatenby JC, Gore JC, Grillon C, et al. (2001) Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci 4: 437-441.
40. Derbyshire SW, Jones AK, Gyulai F, Clark S, Townsend D, et al. (1997) Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain 73: 431-445.
41. Petrovic P, Carlsson K, Petersson KM, Hansson P, Ingvar M (2004) Context-dependent deactivation of the amygdala during pain. J Cogn Neurosci 16: 1289-1301.
42. Petrovic P, Ingvar M, Stone-Elander S, Petersson KM, Hansson P (1999) A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy. Pain 83: 459-470.
43. Rauch SL, Savage CR, Alpert NM, Miguel EC, Baer L, et al. (1995) A positron emission tomographic study of simple phobic symptom provocation. Arch Gen Psychiatry 52: 20-28.
44. Wik G, Fredrikson M, Ericson K, Eriksson L, Stone-Elander S, et al. (1993) A functional cerebral response to frightening visual stimulation. Psychiatry Res 50: 15-24.
45. Campbell LA, Bryant RA (2007) How time flies: a study of novice skydivers. Behav Res Ther 45: 1389-1392.
46. Chatterton RT Jr, Vogelsong KM, Lu YC, Hudgens GA (1997) Hormonal responses to psychological stress in men preparing for skydiving. J Clin Endocrinol Metab 82: 2503-2509.
47. Fenz WD, Epstein S (1967) Gradients of physiological arousal in parachutists as a function of an approaching jump. Psychosom Med 29: 33-51.
48. Schedlowski M, Tewes U (1992) Physiological arousal and perception of bodily state during parachute jumping. Psychophysiology 29: 95-103.
49. Schedlowski M, Benschop RJ, Schmidt RE (1995) Psychological aspects of stress immunology. Immunol Today 16: 165.
50. Schedlowski M, Fluge T, Richter S, Tewes U, Schmidt RE, et al. (1995) Beta-endorphin, but not substance-P, is increased by acute stress in humans. Psychoneuroendocrinology 20: 103-110.
51. Schedlowski M, Jacobs R, Stratmann G, Richter S, Hadicke A, et al. (1993) Changes of natural killer cells during acute psychological stress. J Clin Immunol 13: 119-126.
52. Benschop RJ, Jacobs R, Sommer B, Schurmeyer TH, Raab JR, et al. (1996) Modulation of the immunologic response to acute stress in humans by beta-blockade or benzodiazepines. FASEB J 10: 517-524.
53. Sterlini GL, Bryant RA (2002) Hyperarousal and dissociation: a study of novice skydivers. Behav Res Ther 40: 431-437.
54. Wyatt T (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge: Cambridge University Press.
55. Gallagher P, Leitch MM, Massey AE, McAllister-Williams RH, Young AH (2006) Assessing cortisol and dehydroepiandrosterone (DHEA) in saliva: effects of collection method. J Psychopharmacol 20: 643-649.
56. Natsch A, Gfeller H, Gygax P, Schmid J, Acuna G (2003) A specific bacterial aminoacylase cleaves odorant precursors secreted in the human axilla. J Biol Chem 278: 5718-5727.
57. Preti G, Wysocki CJ, Barnhart KT, Sondheimer SJ, Leyden JJ (2003) Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients. Biol Reprod 68: 2107-2113.
58. Makin HLJ, Trafford DJH, Nolan J (1998) Mass Spectra and GC Data of Steroids. Weinheim, Germany: Wiley-VCH. pp 790.
59. Mackay D, Shiu WY, Sutherland RP (1979) Determination of air-water Henry's law constants for hydrophobic pollutants. Environ Sci Technol 13: 333-337.
60. Lyman WJ, Reehl WF, Rosenblatt DH (1982) Handbook of chemical property estimation methods. New York: McGraw-Hill.
61. de Kock HL, Heinze PH, Potgieter CM, Dijksterhuis GB, Minnaar A (2001) Temporal aspects related to the perception of skatole and androstenone, the major boar odour compounds. Meat Science 57: 61-70.
62. Gower DB, Mallet AI, Watkins WJ, Wallace LM, Calame JP (1997) Capillary gas chromatography with chemical ionization negative ion mass spectrometry in the identification of odorous steroids formed in metabolic studies of the sulphates of androsterone, DHA and 5[alpha]-androst-16-en-3[beta]-ol with human axillary bacterial isolates. J Steroid Biochem Mol Biol 63: 81-89.
63. Lorig TS, Elmes DG, Zald DH, Pardo JV (1999) A computer-controlled olfactometer for fMRI and electrophysiological studies of olfaction. Behav Res Methods Instrum Comput 31: 370-375.
64. Caruso S, Grillo C, Agnello C, Maiolino L, Intelisano G, et al. (2001) A prospective study evidencing rhinomanometric and olfactometric outcomes in women taking oral contraceptives. Hum Reprod 16: 2288-2294.
65. Hummel T, Gollisch R, Wildt G, Kobal G (1991) Changes in olfactory perception during the menstrual cycle. Experientia 47: 712-715.
66. Lundstrom JN, McClintock MK, Olsson MJ (2006) Effects of reproductive state on olfactory sensitivity suggest odor specificity. Biol Psychol 71: 244-247.
67. Mair RG, Bouffard JA, Engen T, Morton TH (1978) Olfactory sensitivity during the menstrual cycle. Sens Processes 2: 90-98.
68. Bremner JD, Steinberg M, Southwick SM, Johnson DR, Charney DS (1993) Use of the Structured Clinical Interview for DSM-IV Dissociative Disorders for systematic assessment of dissociative symptoms in posttraumatic stress disorder. American Journal of Psychiatry 150: 1011-1014.
69. Tabert MH, Steffener J, Albers MW, Kern DW, Michael M, et al. (2007) Validation and optimization of statistical approaches for modeling odorant-induced fMRI signal changes in olfactory-related brain areas. Neuroimage 34: 1375-1390.
70. Poellinger A, Thomas R, Lio P, Lee A, Makris N, et al. (2001) Activation and habituation in olfaction-an fMRI study. Neuroimage 13: 547-560.
71. Sobel N, Prabhakaran V, Zhao Z, Desmond JE, Glover GH, et al. (2000) Time course of odorant-induced activation in the human primary olfactory cortex. J Neurophysiol 83: 537-551.
72. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, et al. (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25: 1325-1335.
73. Newsome WT, Britten KH, Movshon JA (1989) Neuronal correlates of a perceptual decision. Nature 341: 52-54.